Chlorophagy is ATG gene-dependent microautophagy process

Abstract

Autophagy delivers cytosolic components to lysosomes and the vacuole for degradation. This pathway prevents starvation through bulk degradation and recycling of cytoplasmic components, and maintains cellular homeostasis through selective elimination of damaged proteins and organelles. Autophagic delivery processes are categorized into three types: macroautophagy, microautophagy, and chaperone-mediated autophagy. During macroautophagy, nascent, double membrane-bound vesicles termed autophagosomes sequester a portion of cytoplasm and deliver it to the vacuole/lysosomes. Molecular genetic studies in budding yeasts have identified a set of AUTOPHAGY (ATG) genes required for autophagosome formation. Although microautophagy involves the direct lysosomal/vacuolar engulfment and incorporation of a target into the lumen rather than the formation of autophagosomes, the membrane dynamics and possible roles of ATGs during microautophagy are under investigation. Our recent study revealed an ATG-dependent microautophagy process in plants, during which chloroplasts damaged by high visible light (HL) are selectively eliminated. Here, we discuss the membrane dynamics of the plant microautophagy that enables the transport of whole chloroplasts into the vacuole.

Keywords: Autophagy; chlorophagy; chloroplast; microautophagy; photodamage.

Figure 1.

A schematic model of microautophagy in mammalian cells, yeast, and plant cells. (a) Non-selective microautophagy is generally achieved by invagination or protrusion of the lysosomal or vacuolar membrane to incorporate various organelles and proteins. (b) Micropexophagy-specific membrane apparatus (MIPA) structures enclose peroxisomes during micropexophagy in the methylotrophic yeast Komagataella phaffii. (c) High light-damaged chloroplasts exhibiting a swollen shape are selectively eliminated via microautophagy in Arabidopsis leaves. (d) Extension of the vacuolar membrane itself engulfs an anthocyanin aggregate to incorporate it into the vacuole and form anthocyanin vacuolar inclusions (AVIs).

Figure 2.

Images of HL damage-induced swollen chloroplasts in Arabidopsis leaves. (a and b) Confocal images of mesophyll cells expressing stroma-targeted RBCS-RFP under the control of the RBCS promoter along with the vacuolar membrane-targeted GFP-δ-tonoplast intrinsic protein (TIP) under the control of the 35S promoter. The second rosette leaves of non-treated control plants (a) or plants 1 d after exposure to 2-h high visible light (HL; 2,000 µmol m⁻² s⁻¹) at 10℃ (b) were observed. Arrowheads indicate HL-induced swollen chloroplasts. Chlorophyll auto-fluorescence, RFP, and GFP signals appear magenta, green, and turquoise, respectively. DIC images are also shown. Scale Bars = 10 µm.